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Evolution of the germline mutation rate across vertebrates

Author

Listed:
  • Lucie A. Bergeron

    (University of Copenhagen)

  • Søren Besenbacher

    (Aarhus University)

  • Jiao Zheng

    (BGI-Shenzhen
    University of Chinese Academy of Sciences)

  • Panyi Li

    (BGI-Shenzhen)

  • Mads Frost Bertelsen

    (Copenhagen Zoo)

  • Benoit Quintard

    (Parc Zoologique et Botanique de Mulhouse)

  • Joseph I. Hoffman

    (Bielefeld University
    British Antarctic Survey, High Cross)

  • Zhipeng Li

    (Jilin Agricultural University)

  • Judy St. Leger

    (Cornell University)

  • Changwei Shao

    (Chinese Academy of Fishery Sciences)

  • Josefin Stiller

    (University of Copenhagen)

  • M. Thomas P. Gilbert

    (University of Copenhagen
    University Museum, NTNU)

  • Mikkel H. Schierup

    (Aarhus University)

  • Guojie Zhang

    (University of Copenhagen
    Zhejiang University School of Medicine
    Zhejiang University Medical Center
    Chinese Academy of Sciences)

Abstract

The germline mutation rate determines the pace of genome evolution and is an evolving parameter itself1. However, little is known about what determines its evolution, as most studies of mutation rates have focused on single species with different methodologies2. Here we quantify germline mutation rates across vertebrates by sequencing and comparing the high-coverage genomes of 151 parent–offspring trios from 68 species of mammals, fishes, birds and reptiles. We show that the per-generation mutation rate varies among species by a factor of 40, with mutation rates being higher for males than for females in mammals and birds, but not in reptiles and fishes. The generation time, age at maturity and species-level fecundity are the key life-history traits affecting this variation among species. Furthermore, species with higher long-term effective population sizes tend to have lower mutation rates per generation, providing support for the drift barrier hypothesis3. The exceptionally high yearly mutation rates of domesticated animals, which have been continually selected on fecundity traits including shorter generation times, further support the importance of generation time in the evolution of mutation rates. Overall, our comparative analysis of pedigree-based mutation rates provides ecological insights on the mutation rate evolution in vertebrates.

Suggested Citation

  • Lucie A. Bergeron & Søren Besenbacher & Jiao Zheng & Panyi Li & Mads Frost Bertelsen & Benoit Quintard & Joseph I. Hoffman & Zhipeng Li & Judy St. Leger & Changwei Shao & Josefin Stiller & M. Thomas P, 2023. "Evolution of the germline mutation rate across vertebrates," Nature, Nature, vol. 615(7951), pages 285-291, March.
  • Handle: RePEc:nat:nature:v:615:y:2023:i:7951:d:10.1038_s41586-023-05752-y
    DOI: 10.1038/s41586-023-05752-y
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    Cited by:

    1. Juraj Bergman & Rasmus Ø. Pedersen & Erick J. Lundgren & Rhys T. Lemoine & Sophie Monsarrat & Elena A. Pearce & Mikkel H. Schierup & Jens-Christian Svenning, 2023. "Worldwide Late Pleistocene and Early Holocene population declines in extant megafauna are associated with Homo sapiens expansion rather than climate change," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
    2. Sara Ballouz & Risa Karakida Kawaguchi & Maria T. Pena & Stephan Fischer & Megan Crow & Leon French & Frank M. Knight & Linda B. Adams & Jesse Gillis, 2023. "The transcriptional legacy of developmental stochasticity," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    3. Ashley T. Sendell-Price & Frank J. Tulenko & Mats Pettersson & Du Kang & Margo Montandon & Sylke Winkler & Kathleen Kulb & Gavin P. Naylor & Adam Phillippy & Olivier Fedrigo & Jacquelyn Mountcastle & , 2023. "Low mutation rate in epaulette sharks is consistent with a slow rate of evolution in sharks," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    4. Bharat Ravi Iyengar & Anna Grandchamp & Erich Bornberg-Bauer, 2024. "How antisense transcripts can evolve to encode novel proteins," Nature Communications, Nature, vol. 15(1), pages 1-11, December.

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